Design and Characterization of Chemically Stabilized Aβ42 Oligomers

Biochemistry

Volumn 54, Issue 34, 2015, Pages 5315-5321

  Yamin, Ghiam ^a,c   Huynh, Tien Phat Vuong ^b   Teplow, David B ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b WASHINGTON UNIVERSITY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CROSSLINKING; DIMERS; NEURODEGENERATIVE DISEASES; ORGANIC POLYMERS;

ALZHEIMER'S DISEASE; AMYLOID BETAS; CHEMICAL EQUATIONS; DIFFERENT SIZES; FORMAL STRUCTURES; OLIGOMER FORMATIONS; PHOTOCHEMICAL CROSS-LINKING; STRUCTURE ACTIVITY RELATIONSHIPS;

OLIGOMERS;

AMYLOID BETA PROTEIN[1-42]; DIMER; OLIGOMER; PHENYLALANINE; TYROSINE; AMYLOID BETA PROTEIN; AMYLOID BETA-PROTEIN (1-42); CROSS LINKING REAGENT; INTRINSICALLY DISORDERED PROTEIN; PEPTIDE FRAGMENT;

ARTICLE; CROSS LINKING; DISSOCIATION; HUMAN; OLIGOMERIZATION; PATHOGENESIS; PEPTIDE SYNTHESIS; POPULATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN STABILITY; STRUCTURE ACTIVITY RELATION; ALZHEIMER DISEASE; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN ENGINEERING; PROTEIN QUATERNARY STRUCTURE; PROTEINOSIS;

ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMYLOID BETA-PEPTIDES; CROSS-LINKING REAGENTS; HUMANS; INTRINSICALLY DISORDERED PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN ENGINEERING; PROTEIN STABILITY; PROTEIN STRUCTURE, QUATERNARY;

EID: 84940776667     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/acs.biochem.5b00318     Document Type: Article

References (32)

1. Haass, C. and Selkoe, D. J. (2007) Soluble protein oligomers in neurodegeneration: lessons from the Alzheimer's amyloid β-peptide Nat. Rev. Mol. Cell Biol. 8, 101-112 10.1038/nrm2101
2. Dodart, J. C., Meziane, H., Mathis, C., Bales, K. R., Paul, S. M., and Ungerer, A. (1999) Behavioral disturbances in transgenic mice overexpressing the V717F β-amyloid precursor protein Behav. Neurosci. 113, 982-990 10.1037/0735-7044.113.5.982
3. Hsia, A. Y., Masliah, E., McConlogue, L., Yu, G. Q., Tatsuno, G., Hu, K., Kholodenko, D., Malenka, R. C., Nicoll, R. A., and Mucke, L. (1999) Plaque-independent disruption of neural circuits in Alzheimer's disease mouse models Proc. Natl. Acad. Sci. U. S. A. 96, 3228-3233 10.1073/pnas.96.6.3228
4. Moechars, D., Dewachter, I., Lorent, K., Reverse, D., Baekelandt, V., Naidu, A., Tesseur, I., Spittaels, K., Haute, C. V., Checler, F., Godaux, E., Cordell, B., and Van Leuven, F. (1999) Early phenotypic changes in transgenic mice that overexpress different mutants of amyloid precursor protein in brain J. Biol. Chem. 274, 6483-6492 10.1074/jbc.274.10.6483
5. Moechars, D., Lorent, K., and Van Leuven, F. (1999) Premature death in transgenic mice that overexpress a mutant amyloid precursor protein is preceded by severe neurodegeneration and apoptosis Neuroscience 91, 819-830 10.1016/S0306-4522(98)00599-5
6. Kumar-Singh, S., Dewachter, I., Moechars, D., Lubke, U., De Jonghe, C., Ceuterick, C., Checler, F., Naidu, A., Cordell, B., Cras, P., Van Broeckhoven, C., and Van Leuven, F. (2000) Behavioral disturbances without amyloid deposits in mice overexpressing human amyloid precursor protein with Flemish (A692G) or Dutch (E693Q) mutation Neurobiol. Dis. 7, 9-22 10.1006/nbdi.1999.0272
7. 1-42 in wild-type human amyloid protein precursor transgenic mice: Synaptotoxicity without plaque formation J. Neurosci. 20, 4050-4058
8. Fancy, D. A. and Kodadek, T. (1999) Chemistry for the analysis of protein-protein interactions: Rapid and efficient cross-linking triggered by long wavelength light Proc. Natl. Acad. Sci. U. S. A. 96, 6020-6024 10.1073/pnas.96.11.6020
9. Bitan, G., Kirkitadze, M. D., Lomakin, A., Vollers, S. S., Benedek, G. B., and Teplow, D. B. (2003) Amyloid β-protein (Aβ) assembly: Aβ40 and Aβ42 oligomerize through distinct pathways Proc. Natl. Acad. Sci. U. S. A. 100, 330-335 10.1073/pnas.222681699
10. Ono, K., Condron, M. M., and Teplow, D. B. (2009) Structure-neurotoxicity relationships of amyloid β-protein oligomers Proc. Natl. Acad. Sci. U. S. A. 106, 14745-14750 10.1073/pnas.0905127106
11. Roychaudhuri, R., Yang, M., Hoshi, M. M., and Teplow, D. B. (2009) Amyloid β-protein assembly and Alzheimer disease J. Biol. Chem. 284, 4749-4753 10.1074/jbc.R800036200
12. Lazo, N. D., Grant, M. A., Condron, M. C., Rigby, A. C., and Teplow, D. B. (2005) On the nucleation of amyloid β-protein monomer folding Protein Sci. 14, 1581-1596 10.1110/ps.041292205
13. Maji, S. K., Ogorzalek Loo, R. R., Inayathullah, M., Spring, S. M., Vollers, S. S., Condron, M. M., Bitan, G., Loo, J. A., and Teplow, D. B. (2009) Amino acid position-specific contributions to amyloid β-protein oligomerization J. Biol. Chem. 284, 23580-23591 10.1074/jbc.M109.038133
14. Walsh, D. M., Hartley, D. M., Kusumoto, Y., Fezoui, Y., Condron, M. M., Lomakin, A., Benedek, G. B., Selkoe, D. J., and Teplow, D. B. (1999) Amyloid β-protein fibrillogenesis. Structure and biological activity of protofibrillar intermediates J. Biol. Chem. 274, 25945-25952 10.1074/jbc.274.36.25945
15. Bitan, G. and Teplow, D. B. (2004) Rapid photochemical cross-linking - A new tool for studies of metastable, amyloidogenic protein assemblies Acc. Chem. Res. 37, 357-364 10.1021/ar000214l
16. Cleveland, D. W., Fischer, S. G., Kirschner, M. W., and Laemmli, U. K. (1977) Peptide mapping by limited proteolysis in sodium dodecyl sulfate and analysis by gel electrophoresis J. Biol. Chem. 252, 1102-1106
17. Kirkitadze, M. D., Bitan, G., and Teplow, D. B. (2002) Paradigm shifts in Alzheimer's disease and other neurodegenerative disorders: The emerging role of oligomeric assemblies J. Neurosci. Res. 69, 567-577 10.1002/jnr.10328
18. Klein, W. E. (2006) Cytotoxic intermediates in the fibrillation pathway: Aβ oligomers in Alzheimer's disease as a case study. In Part A: Protein Misfolding, Aggregation, and Conformational Diseases (Uversky, V. N. and Fink, A. L., Eds.) pp 61-75, Springer, New York.
19. Bitan, G., Vollers, S. S., and Teplow, D. B. (2003) Elucidation of primary structure elements controlling early amyloid β-protein oligomerization J. Biol. Chem. 278, 34882-34889 10.1074/jbc.M300825200
20. Bitan, G., Lomakin, A., and Teplow, D. B. (2001) Amyloid β-protein oligomerization: prenucleation interactions revealed by photo-induced cross-linking of unmodified proteins J. Biol. Chem. 276, 35176-35184 10.1074/jbc.M102223200
21. Diociaiuti, M., Macchia, G., Paradisi, S., Frank, C., Camerini, S., Chistolini, P., Gaudiano, M. C., Petrucci, T. C., and Malchiodi-Albedi, F. (2014) Native metastable prefibrillar oligomers are the most neurotoxic species among amyloid aggregates Biochim. Biophys. Acta, Mol. Basis Dis. 1842, 1622-1629 10.1016/j.bbadis.2014.06.006
22. Meyer, J. P., Pelton, J. T., Hoflack, J., and Saudek, V. (1991) Solution structure of salmon calcitonin Biopolymers 31, 233-241 10.1002/bip.360310210
23. Roychaudhuri, R., Yang, M., Deshpande, A., Cole, G. M., Frautschy, S., Lomakin, A., Benedek, G. B., and Teplow, D. B. (2013) C-terminal turn stability determines assembly differences between Aβ40 and Aβ42 J. Mol. Biol. 425, 292-308 10.1016/j.jmb.2012.11.006
24. Maji, S. K., Amsden, J. J., Rothschild, K. J., Condron, M. M., and Teplow, D. B. (2005) Conformational dynamics of amyloid β-protein assembly probed using intrinsic fluorescence Biochemistry 44, 13365-13376 10.1021/bi0508284
25. Urbanc, B., Betnel, M., Cruz, L., Bitan, G., and Teplow, D. B. (2010) Elucidation of amyloid β-protein oligomerization mechanisms: discrete molecular dynamics study J. Am. Chem. Soc. 132, 4266-4280 10.1021/ja9096303
26. Chen, W. T., Hong, C. J., Lin, Y. T., Chang, W. H., Huang, H. T., Liao, J. Y., Chang, Y. J., Hsieh, Y. F., Cheng, C. Y., Liu, H. C., Chen, Y. R., and Cheng, I. H. (2012) Amyloid-β (Aβ) D7H mutation increases oligomeric Aβ42 and alters properties of Aβ-zinc/copper assemblies PLoS One 7, e35807 10.1371/journal.pone.0035807
27. Sugiki, T. and Utsunomiya-Tate, N. (2013) Site-specific aspartic acid isomerization regulates self-assembly and neurotoxicity of amyloid-β Biochem. Biophys. Res. Commun. 441, 493-498 10.1016/j.bbrc.2013.10.084
28. Yang, M. and Teplow, D. B. (2008) Amyloid β-protein monomer folding: free-energy surfaces reveal alloform-specific differences J. Mol. Biol. 384, 450-464 10.1016/j.jmb.2008.09.039
29. Oosawa, F., Asakura, S., and Ooi, T. (1961) Physical Chemistry of Muscle Protein "Actin" Prog. Theor. Phys. Suppl. 17, 14-34 10.1143/PTPS.17.14
30. Oosawa, F. and Kasai, M. (1962) A theory of linear and helical aggregations of macromolecules J. Mol. Biol. 4, 10-21 10.1016/S0022-2836(62)80112-0
31. Murray, M. M., Bernstein, S. L., Nyugen, V., Condron, M. M., Teplow, D. B., and Bowers, M. T. (2009) Amyloid β-protein: Aβ40 inhibits Aβ42 oligomerization J. Am. Chem. Soc. 131, 6316-6317 10.1021/ja8092604
32. Bernstein, S. L., Dupuis, N. F., Lazo, N. D., Wyttenbach, T., Condron, M. M., Bitan, G., Teplow, D. B., Shea, J. E., Ruotolo, B. T., Robinson, C. V., and Bowers, M. T. (2009) Amyloid-β protein oligomerization and the importance of tetramers and dodecamers in the aetiology of Alzheimer's disease Nat. Chem. 1, 326-331 10.1038/nchem.247